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. 2024 Sep 28;24(1):373.
doi: 10.1186/s12866-024-03531-x.

Symbiotic bacteria Sodalis glossinidius, Spiroplasma sp and Wolbachia do not favour Trypanosoma grayi coexistence in wild population of tsetse flies collected in Bobo-Dioulasso, Burkina Faso

Youssouf Mouliom Mfopit  1   2   3 , Etienne Bilgo  4   5   6 , Soudah Boma  7 , Martin Bienvenu Somda  7   8 , Jacques Edounou Gnambani  5   6 , Maurice Konkobo  5   6 , Abdoulaye Diabate  4   5   6 , Guiguigbaza-Kossigan Dayo  7 , Mohammed Mamman  9   10 , Soerge Kelm  11 , Emmanuel Oluwadare Balogun  12   9 , Mohammed Nasir Shuaibu  12   9 , Junaidu Kabir  9   13
Affiliations

Symbiotic bacteria Sodalis glossinidius, Spiroplasma sp and Wolbachia do not favour Trypanosoma grayi coexistence in wild population of tsetse flies collected in Bobo-Dioulasso, Burkina Faso

Youssouf Mouliom Mfopit et al. BMC Microbiol. .

Abstract

Background: Tsetse flies, the biological vectors of African trypanosomes, have established symbiotic associations with different bacteria. Their vector competence is suggested to be affected by bacterial endosymbionts. The current study provided the prevalence of three tsetse symbiotic bacteria and trypanosomes in Glossina species from Burkina Faso.

Results: A total of 430 tsetse flies were captured using biconical traps in four different collection sites around Bobo-Dioulasso (Bama, Bana, Nasso, and Peni), and their guts were removed. Two hundred tsetse were randomly selected and their guts were screened by PCR for the presence of Sodalis glossinidius, Spiroplasma sp., Wolbachia and trypanosomes. Of the 200 tsetse, 196 (98.0%) were Glossina palpalis gambiensis and 4 (2.0%) Glossina tachinoides. The overall symbiont prevalence was 49.0%, 96.5%, and 45.0%, respectively for S. glossinidius, Spiroplasma and Wolbachia. Prevalence varied between sampling locations: S. glossinidius (54.7%, 38.5%, 31.6%, 70.8%); Spiroplasma (100%, 100%, 87.7%, 100%); and Wolbachia (43.4%, 38.5%, 38.6%, 70.8%), respectively in Bama, Bana, Nasso and Peni. Noteworthy, no G. tachnoides was infected by S. glossinidius and Wolbachia, but they were all infected by Spiroplasma sp. A total of 196 (98.0%) harbored at least one endosymbionts. Fifty-five (27.5%) carried single endosymbiont. Trypanosomes were found only in G. p. gambiensis, but not G. tachinoides. Trypanosomes were present in flies from all study locations with an overall prevalence of 29.5%. In Bama, Bana, Nasso, and Peni, the trypanosome infection rate was respectively 39.6%, 23.1%, 8.8%, and 37.5%. Remarkably, only Trypanosoma grayi was present. Of all trypanosome-infected flies, 55.9%, 98.3%, and 33.9% hosted S. glossinidius, Spiroplasma sp and Wolbachia, respectively. There was no association between Sodalis, Spiroplasma and trypanosome presence, but there was a negative association with Wolbachia presence. We reported 1.9 times likelihood of trypanosome absence when Wolbachia was present.

Conclusion: This is the first survey reporting the presence of Trypanosoma grayi in tsetse from Burkina Faso. Tsetse from these localities were highly positive for symbiotic bacteria, more predominantly with Spiroplasma sp. Modifications of symbiotic interactions may pave way for disease control.

Keywords: Sodalis glossinidius; Spiroplasma; Trypanosoma grayi; Wolbachia; Burkina Faso; Tsetse flies.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1
Map of study area. Trapping sites are marked with yellow squares. Tsetse flies were collected in Bama (10 traps), Bana (5 traps), Nasso (5 traps) and Peni (10 traps) (Map created with mapchart.net and SW Map)
Fig. 2
Fig. 2
Phylogenetic analysis of S. glossinidius hemolysin partial gene sequence and its close relatives. Our isolate is marked by a black diamond. The evolutionary history conducted in MEGA X [33] was inferred by using the Maximum Likelihood method and Kimura 2-parameter model [34]. The tree with the highest log likelihood (-1896.54) is shown. The percentage of trees in which the associated taxa clustered together is shown next to the branches. This analysis involved 13 nucleotide sequences
Fig. 3
Fig. 3
Phylogenetic analysis of Spiroplasma 16S rRNA partial gene sequence and its close relatives. Our isolate is marked by a black diamond. The evolutionary history conducted in MEGA X [33] was inferred by using the Maximum Likelihood method and Kimura 2-parameter model [34]. The tree with the highest log likelihood (-927.62) is shown. The percentage of trees in which the associated taxa clustered together is shown next to the branches. This analysis involved 17 nucleotide sequences. There were a total of 307 positions in the final dataset
Fig. 4
Fig. 4
Phylogenetic analysis of Wolbachia 16S rRNA partial gene sequence and its close relatives. Our isolate is marked by a black diamond. The evolutionary history conducted in MEGA X [33], was inferred by using the Maximum Likelihood method and Kimura 2-parameter model [34]. The tree with the highest log likelihood (-732.22) is shown. The percentage of trees in which the associated taxa clustered together is shown next to the branches. This analysis involved 13 nucleotide sequences. There were a total of 331 positions in the final dataset
Fig. 5
Fig. 5
Coexistence of Sodalis, Spiroplasma, and Wolbachia. Endosymbionts co-existed in 141 tsetse flies. A total of 97 flies carried double infections: Spiroplasma + Wolbachia (43), Sodalis + Wolbachia (1), Sodalis + Spiroplasma (53), and 44 triple infection (Sodalis + Spiroplasma + Wolbachia)
Fig. 6
Fig. 6
Agarose gel of selected ITS-1 amplicons. Lane M: Molecular Marker 100 bp; Lane 1: T. grayi; Lane 2: T. grayi; Lane 3: T. grayi and kinetoplastid; Lane 4: T. grayi and kinetoplastid; Lane 5: T. grayi and kinetoplastid; Lane 6: T. grayi; Lane P: Positive control; Lane 7: T. grayi and kinetoplastid; Lane N: Negative control
Fig. 7
Fig. 7
Phylogenetic analysis of Trypanosoma and kinetoplastidae ITS-1 gene sequences. Our isolate is marked by a black diamond. The evolutionary history conducted in MEGA X [33], was inferred by using the Maximum Likelihood method and Kimura 2-parameter model [34]. The tree with the highest log likelihood (-1054.41) is shown. The percentage of trees in which the associated taxa clustered together is shown next to the branches. A discrete Gamma distribution was used to model evolutionary rate differences among sites. This analysis involved 14 nucleotide sequences
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